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Emerging infectious diseases (EIDs) have contributed significantly to the current biodiversity crisis, leading to widespread epidemics and population loss. Owing to genetic variation in pathogen virulence, a complete understanding of species decline requires the accurate identification and characterization of EIDs. We explore this issue in the Western honeybee, where increasing mortality of populations in the Northern Hemisphere has caused major concern. Specifically, we investigate the importance of genetic identity of the main suspect in mortality, deformed wing virus (DWV), in driving honeybee loss. Using laboratory experiments and a systematic field survey, we demonstrate that an emerging DWV genotype (DWV-B) is more virulent than the established DWV genotype (DWV-A) and is widespread in the landscape. Furthermore, we show in a simple model that colonies infected with DWV-B collapse sooner than colonies infected with DWV-A. We also identify potential for rapid DWV evolution by revealing extensive genome-wide recombination in vivo. The emergence of DWV-B in naive honeybee populations, including via recombination with DWV-A, could be of significant ecological and economic importance. Our findings emphasize that knowledge of pathogen genetic identity and diversity is critical to understanding drivers of species decline.
Emerging infectious diseases (EIDs) have contributed significantly to the current biodiversity crisis, leading to widespread epidemics and population loss. Owing to genetic variation in pathogen virulence, a complete understanding of species decline requires the accurate identification and characterization of EIDs. We explore this issue in the Western honeybee, where increasing mortality of populations in the Northern Hemisphere has caused major concern. Specifically, we investigate the importance of genetic identity of the main suspect in mortality, deformed wing virus (DWV), in driving honeybee loss. Using laboratory experiments and a systematic field survey, we demonstrate that an emerging DWV genotype (DWV-B) is more virulent than the established DWV genotype (DWV-A) and is widespread in the landscape. Furthermore, we show in a simple model that colonies infected with DWV-B collapse sooner than colonies infected with DWV-A. We also identify potential for rapid DWV evolution by revealing extensive genome-wide recombination in vivo. The emergence of DWV-B in naive honeybee populations, including via recombination with DWV-A, could be of significant ecological and economic importance. Our findings emphasize that knowledge of pathogen genetic identity and diversity is critical to understanding drivers of species decline.
Social bees, lower termites and pathogens: eclectic research in social insect evolution and ecology
(2015)
A fundamental yet seemingly contradictory aspect of biological individuals is their capacity to remain the same while changing through time. This self-regulatory ability is facilitated by a number of factors that are shared by all complex multicellular life-forms. One such essential trait is an effective immune system. Here, I use concepts of individuality and immunity to explore the blurred line between society and individual in termite “superorganisms”. I discuss our current understanding of the breadth and mechanistic underpinnings of collective immunity in termites, before going on to explore the evolution of the immune system during the transition from a cockroach-like ancestor to a fully-fledged termite society. I end by discussing the possibly crucial role played by immunity during the emergence of eusociality, and in transitions in organismal complexity generally.
The evolution and mechanistic underpinnings of termite immunity are not well understood. Given the intimate relationship between sociality and disease, this represents a major gap in understanding, particularly since termites represent the only animal group outside of Hymenoptera to have evolved such advanced forms of social living. We explore the evolution of termite immunity by conducting qualitative and quantitative transcriptomic analyses from twelve cockroach and termite species occurring along a gradient of sociality. We incorporate lineages spanning the origin of eusociality, and include species from a key transitional subsocial group: the wood roaches. Firstly, we analyze immune characteristics in the context of termite phylogeny. Here, we examine the evolution of immune traits during the transition to eusociality, and explore the extent to which immune adaptations are associated with evolutionary shifts in social complexity and ecology. Secondly, we conduct a quantitative analysis of responses to a common immune stimulus to examine the role of both sociality and caste in immunity. Here, we test the hypothesis that the evolution of division of labour – and associated increases in investment into costly altruistic (immune) traits – occurred at the expense of individual immunity in the sterile caste.
The evolution and mechanistic underpinnings of termite immunity are not well understood. Given the intimate relationship between sociality and disease, this represents a major gap in understanding, particularly since termites represent the only animal group outside of Hymenoptera to have evolved such advanced forms of social living. We explore the evolution of termite immunity by conducting qualitative and quantitative transcriptomic analyses from twelve cockroach and termite species occurring along a gradient of sociality. We incorporate lineages spanning the origin of eusociality, and include species from a key transitional subsocial group: the wood roaches. Firstly, we analyze immune characteristics in the context of termite phylogeny. Here, we examine the evolution of immune traits during the transition to eusociality, and explore the extent to which immune adaptations are associated with evolutionary shifts in social complexity and ecology. Secondly, we conduct a quantitative analysis of responses to a common immune stimulus to examine the role of both sociality and caste in immunity. Here, we test the hypothesis that the evolution of division of labour – and associated increases in investment into costly altruistic (immune) traits – occurred at the expense of individual immunity in the sterile caste.
Social insects nesting in soil environments are in constant contact with entomopathogens and have evolved disease resistance mechanisms within a colony to prevent the occurrence and spread of infectious diseases. Among these mechanisms: mutual grooming reduces the cuticular load of pathogens, and burial of cadavers and cannibalism can prevent pathogens from replicating within the group. We explored how the rate and type of collective behavioural response is determined by stepwise infection dynamics operating at the level of the individual. Specifically, we infected the eastern subterranean termite Reticulitermes flavipes with different types of infectious particle and infection route of the entomopathogenic fungus Metarhizium anisopliae and recorded behavioural responses of nestmates to individuals at different times during the progression of infections. As expected, termites groomed conidia-exposed individuals significantly more than controls. Interestingly, grooming was significantly elevated after fungal germination than before, suggesting that pathogen growth cues act as strong stimulators of allogrooming. Conidia-exposed termites were cannibalized, but only after they became visibly ill. By contrast, termites did not groom blastospore-injected individuals more than controls at any time-point following infection. Instead, we found that blastospore-injected individuals were continually cannibalized at a low-level following injection with either viable or heat-killed blastospores, with a marked increase in cannibalism after termites injected with viable blastospores became visibly ill and were close to death. Together, these findings point to the importance of host condition as a cue for social hygienic behavior, and that the host itself appears to emit essential sickness cues that act as targets for its own sacrifice. This demonstrates that termites have independently evolved to both identify and destructively respond to sickness.
The termites are a derived eusocial lineage of otherwise non-social cockroaches. Understanding the proximal and ultimate drivers of this major evolutionary transition represents an important goal in biology. One outstanding question concerns the evolution of termite immunity, which is thought to have undergone broad-sweeping adaptations in order to enhance group-level immune protection. To understand the evolutionary origins of termite immunity, we conducted qualitative and quantitative transcriptome analyses along a gradient of sociality. Firstly, we aimed to identify large-scale genetic shifts in immune traits linked to eusociality by comparing immune gene repertoires in solitary and subsocial cockroaches and across a range of eusocial termite lineages. Secondly, we compared the responses of a solitary cockroach, a subsocial wood-roach and different castes of a lower termite species to a non-specific immune challenge, in order to understand how sociality may have influenced the evolution of immune gene regulation. Firstly, we found that termites have a broadly representative repertoire of canonical immune genes as compared to gregarious cockroaches and subsocial wood-roaches. Secondly, with respect to immune challenge, the solitary cockroach and the subsocial wood-roach displayed a similarly comprehensive induced response, while the termite response was considerably dampened by comparison and strongly influenced by caste; with reproductives displaying a generally higher constitutive level of immune-gene expression compared to sterile castes. In summary we did not find termite eusociality to be associated with significant changes in immune gene diversity, but rather to be linked with significant modifications to the regulation of immunity following the origin of division of labour.